Acute effect of transcranial direct current stimulation (tDCS) on postural control of trained athletes: A randomized controlled trial

Transcranial direct current stimulation (tDCS) is used to modulate brain function, and can modulate motor and postural control. While the acute effect of tDCS is well documented on patients, little is still known whether tDCS can alter the motor control of healthy trained participants. This study aimed to assess the acute effect of tDCS on postural control of parkour practitioners, known for their good balance abilities and their neuromuscular specificities that make them good candidates for tDCS intervention. Eighteen parkour practitioners were tested on three occasions in the laboratory for each stimulation condition (2 mA; 20 minutes)–primary motor cortex (M1), dorsolateral prefrontal cortex (dlPFC) and sham (placebo). Postural control was evaluated PRE and POST each stimulation by measuring Center of Pressure (CoP) displacements on a force platform during static conditions (bipedal and unipedal stance). Following M1 stimulation, significant decreases were observed in CoP area in unipedal (from 607.1 ± 297.9 mm2 to 451.1 ± 173.9 mm2, P = 0.003) and bipedal (from 157.5 ± 74.1 mm2 to 117.6 ± 59.8 mm2 P<0.001) stances. As well, the CoP total length was significantly reduced in bipedal (from 3416.8 ± 295.4 mm to 3280.6 ± 306.2 mm, P = 0.005) as well as in unipedal stance (from 4259.6 ± 398.4 mm to 3846.5 ± 468.9 mm, P<0.001), only after M1 stimulation. Relative pre-post changes observed after M1 stimulation were negatively correlated to experience in parkour only after unipedal stance (r = 0.715, P<0.001), meaning that the more participants were trained the less tDCS was effective. No significant changes were noticed after sham and dlPFC stimulation. These results suggested that the modulation of gait performance in athletes following an acute intervention of tDCS is specific to the targeted brain region, and that postures with reduced base of support (such as unipedal stance) were more sensitive to tDCS.


Introduction
Postural control requires the interaction of several brain regions, including the motor and premotor cortex, the sensorimotor cortex, the basal ganglia, the thalamus, the fronto-parietal regions and the cerebellum [1].Among the methods that improve balance, non-invasive brain stimulation has been suggested as a good alternative to improve motor skills or optimize rehabilitation programs [2].Transcranial direct current stimulation (tDCS) consists of delivering a constant low intensity current (1 to 4 mA) evoked by an electrode (the anode) and directed towards a second electrode (the cathode).Through this process, tDCS is able to modulate neural activity of the cortical crossed areas [3].The literature about tDCS and postural control has mainly focused on the primary motor cortex, showing improvement either during [4] or after the stimulation [5,6].It is suggested that modulating M1 excitability might improve balance by modulating cortico-muscular coherence in ankle muscles [4,7].However, another brain region is often targeted in tDCS literature: the left dorsolateral prefrontal cortex (dlPFC).So far, this brain region is mostly targeted for the improvement of cognitive functions such as attention [8] or memory [9].The dlPFC is also a frequent target to evaluate whether tDCS can improve motor performance, mostly related to whole-body and/or single joint endurance [10,11], but also to fine motor skills during reaching or pointing tasks [12,13].There already exist some clues in the literature, although much less than for M1, that stimulation of the dlPFC also appears likely to improve postural control in young recreationally active adults [14].Indeed, several recent structural and functional neuroimaging studies showed that dlPFC is involved in the control of standing and locomotion [15].
Most previous works on the tDCS effect on postural control included untrained subjects with no specific skills in balance, questioning if tDCS could work on pre-existant circuitry or if a ceiling effect could be observed on more experienced participants.It is well known that sport practice leads to refine postural control [16].In the present study, we aimed to include athletes that are particularly trained regarding balance-parkour practitioners [17].Parkour is a modern physical activity which consists in overcoming various obstacles from the urban landscape, such as fences, benches, or walls [18].Parkour practitioners (also called traceurs) showed greater lower limb muscle performances than untrained individuals or other trained athletes such as track and field athletes or gymnasts, particularly in eccentric modality [19].These performances were accompanied by a greater cortico-spinal excitability and a different spinal/cortical activation pattern in traceurs than in untrained individuals, attributed to the particular motor control required by parkour practice [20].Proprioception and balance are therefore widely used by traceurs, leading them to have a better perception of their body in space in comparison to recreationally active individuals [17].This last point also allows to counterbalance the possible lack of visual information and justifies that traceurs have a significantly lower Centre of Pressure (CoP) surface area with their eyes closed than recreationally active subjects [17].Besides, Parkour offers a particular dynamic postural stability-especially when performing precision landings [21] for which practitioners develop a more stable compensatory movement to counteract the impact at landing, with a lower excursion of the CoP than sedentary subjects.We previously demonstrated that tDCS acutely applied over M1 led to a significant improvement of jump abilities of traceurs [12].Conversely, tDCS applied over dlPFC did not lead to jump improvement but refined the management of fine motor tasks, i.e. accurate pointing tasks [12].Therefore, managing posture is at the interface of a whole-body performance such as jumping and a fine motor control strategy showing that either dlPFC or M1 stimulation could possibly modify balance ability in parkour practitioners.
In this context, we aimed to assess the acute effect of tDCS applied on two brain regions classically stimulated in the literature (M1 and the left dlPFC) on postural control of athletes with well-known balance abilities.Furthermore, the specificity of corticospinal and spinal networks plasticity induced by parkour practice [20,22] might make parkour practitioners potentially good responder for tDCS intervention.Indeed, a modulation of spinal excitability and descending command of triceps surae muscles, particularly involved in posture, by anodal tDCS has already been found in traceurs [23].Mostly because of a potential ceiling effect, the effect of tDCS might be different according to the level of expertise of the participants as studied in previous literature, and particularly the brain region of interest.We therefore conducted a double-blinded, sham-controlled trial performed by recruiting participants with various experience in Parkour, from beginners to well-trained athletes.It was suggested that tDCS effects can be widely influenced by many factors, including the type and amount of previous sport practice [24].Given that this population present pre-cabled cortical circuits to regulate balance, we hypothesized that tDCS may have a significant effect on postural control of Parkour athletes.However, a ceiling effect could be expected on the most experienced individuals as suggested in previous experiments on power-lifters [25] or endurance athletes [26].To that aim we correlated experience of the tested individuals (in total training volume) to the effect of tDCS (in percentage of gains provided by tDCS, by determining Pearson's r.Then, we also hypothesized that tDCS might have lower effect in the most trained individuals.

Participants
Eighteen healthy young males (age: 22.6 ± 5.7 years old; height: 180 ± 5.7 cm; weight: 74.5 ± 7.8 kg) gave their written informed consent to participate in the present study.Participants reported a regular practice of Parkour, at a wide range of expertise.Our sample size calculation was based on changes in motor performance before and after a tDCS session during an explosive task (jumps) [27].Considering a significance level of 5%, a power of 90%, and a standard deviation for paired differences of 6.5 (calculated from standard deviations with an hypothesis of a covariance of measures of 50%), 15 jumpers are needed to meet the objectives of the study.Sample size calculation was performed on PASS 13 Power Analysis and Sample Size Software (2014) [28].Their total training volume (in hours), estimated with their experience (in years) and training frequency (in hours/week) has been evaluated and ranged from 156 to 10,608 hours (mean: 4343 ± 3508).Data were collected from May 2019 to May 2021, and accessed May 2021.Research protocol was approved by the regional ethic committee (CPP-Est-IV) under the number 18/47, registered on ClinicalTrials.org(NCT03937115), and conducted in accordance with the last version of the Declaration of Helsinki.

Experimental set-up and procedures
This study was a double-blinded, randomized, sham-controlled trial to determine the effects of tDCS applied over M1 or dlPFC on static and dynamic balance of Parkour practitioners.The protocol was carried out in 3 experimental sessions separated by at least 48h.The following conditions were performed randomly-anodal tDCS over right M1, anodal tDCS over dlPFC and sham stimulation.The randomization was done at the visit level, meaning that the order of the sessions was randomly assigned for each participant.To ensure the blinding of the type of tDCS applied toward participants, participants were told that any of the three experimental conditions could be a placebo session, independently of the electrode placement.Participants were asked after each session to report if they felt the stimulation was active or placebo.Most subjects (55.6%) thought they had received active stimulation during the placebo session.No difference has been reported in adverse events experienced (tingling, itching, etc.) between the placebo and the active sessions.During each session, subjects performed postural tasks on a force plate before and after tDCS intervention.They executed a bipedal and unipedal static posture before and after tDCS conditions.Similar tests were performed in PRE and POST measurements, but the testing order was randomized across conditions and participants.

Assessment of static posture
Static posture was appraised by means of two experimental conditions-bipedal and unipedal stance, performed on a force plate (Kistler Instrument Corp., Winterthur, Switzerland).The force plate allowed continuous recording of CoP displacements (sampling frequency: 1000 Hz) in both medio-lateral and postero-anterior axis.Bipedal stance was assessed by asking participants to stand still on the force plate, feet shoulder-width apart and arms relaxed.Unipedal stance was evaluated by asking participants to stand still on the left foot by bending the knee of the right leg.Contact with the supporting leg was not allowed.Foot placement and spacing was measured during the first session to be reproduced in the two others.In the two postural conditions, 30 seconds recording were performed, during which participants were asked to keep quiet, eyes open.The last 20 seconds were taken for analysis.

Transcranial direct current stimulation
tDCS was delivered by a neurostimulation device (StarStim1, Neuroelectrics©, Barcelona, Spain) adapted to double-blind procedure.It was transmitted by two saline-soaked synthetic sponge electrodes (Sponstim1, 25cm 2 ) placed on the scalp or shoulder.Every participant agreed to undergo three 20-minute sessions of tDCS (two actives and one sham), separated by 48 hours.Electrodes placement was carried out using the international EEG 10/20 system.The experiment included three stimulation sequences: (i) anode facing the dlPFC (F3 position) and cathode facing the right supra-orbital region (AF8 position), (ii) anode over the dlPFC (F3) and cathode facing the right supra-orbital region (AF8), which is related to sham condition, and (iii) anode facing the right M1 (FC2 position) and cathode placed on the left shoulder.Sequence order was randomized by computer beforehand.Participants were told that any of the three conditions, even including different electrode montages, could be a SHAM condition.During active stimulation conditions, a 2 mA current was generated.The sham condition corresponds to a gradual increase in the intensity of the current during the first 30

Data analysis
First of all, no missing data has to be reported in the whole data set.In static conditions, i.e. bipedal and unipedal upright standing, CoP characteristics were analyzed taking the 20 seconds trial as a whole.The force-plate represents a two-dimensional plane in which the x-axis represents the postero-anterior axis and the y axis the medio-lateral axis, since participants were always oriented in the same direction.The total sway path (length of CoP displacement) has been determined as the total distance covered by the CoP during the 20 seconds of interest.The area of CoP displacements was also analyzed as the area of the ellipse that includes 90% of CoP points for 20 seconds.Postero-anterior and medio-lateral amplitudes were determined as the maximal amplitude (maximal value-minimal value) covered by the CoP in the ellipse area in the x-axis and y-axis, respectively.
The relationship between these CoP variables and training volume of the participants (in hours, see "participants" section) were evaluated by determining the coefficient of correlation (Pearson's correlation) to test the effect of experience on postural control.
The relative changes in CoP variables with the different tDCS intervention were determined in percentage by the following formula: [(POST-PRE)/PRE]*100.These relative changes plotted against training volume or initial performance (averaged PRE value).

Statistical analysis
All data are presented as the mean ± standard deviation (S.D.).Each test (unipedal, bipedal) was considered separately.The normality of the data sets was verified by the Shapiro-Wilk test, and variance homogeneity by the Levene test.Outcome variables tested were, in both bipedal and unipedal standing: CoP length (mm), CoP area (mm 2 ), antero-posterior amplitude of CoP displacement (mm), medio-lateral amplitude of CoP displacement (mm).Two-way repeated measures ANOVA were used to assess differences between the 3 conditions with factors "time" (pre, post) and "tDCS intervention" (M1, dlPFC, SHAM).A one-way repeated measures ANOVA was performed on the relative changes, with factor "tDCS intervention" (M1, dlPFC, SHAM).Post-hoc tests were performed with Bonferroni test.Relationships between the several variables were assessed through Pearson's coefficient of correlation.To account for session order effect (since tDCS conditions were performed randomly), two-way repeated measures ANOVA were also used to assess differences between the 3 conditions in their chronological order with factors "time" (pre, post) and "number of the session" (first, second, third).Effects size are indicated as the partial eta square (ƞ 2 p), Statistical analysis was performed using STATISTICA (10.0 version, Statsoft, Tulsa, Okhlaoma, USA).The level of statistical significance was set at P < 0.05.

Results
Regarding a potential confounding factor due to the three separate days of testing, we carefully checked the baseline measurement during each session.No difference was found in any parameter (CoP length, CoP area, antero-posterior amplitude of CoP displacement, medio-lateral amplitude of CoP displacement) regarding differences between the PRE data of each experimental session.Similarly, no session-order effect was found when analyzing data chronologically, regardless of the tDCS intervention.
No significant changes in CoP length and area have been observed for both sham and dlPFC conditions, in both bidepal and unipedal stance (Fig 1A -1D).Following M1 stimulation, significant decreases were observed in CoP length from PRE to POST in bipedal stance (P = 0.004) and unipedal stance (P = 0.003).As well, significant decreases were also observed in CoP area (P<0.001 and P = 0.002 for bidepal and unipedal stances, respectively).All statistic results are presented in Table 1.
In bidepal stance, a significant decrease from PRE to POST has been observed after M1 stimulation in postero-anterior amplitude of CoP displacement (P = 0.043), while no change has been observed in mediolateral axis (Fig 1E).In unipedal stance, significant decrease of postero-anterior amplitude (P = 0.003) has been observed, while mediolateral amplitude decreased (P = 0.005), both after M1 stimulation only (Fig 1F).No significant changes in amplitudes have been observed from PRE to POST in both sham and dlPFC conditions.
It can be noticed that relationships have been established between CoP characteristics and level of expertise of the participants.First, both CoP lengths and area were significantly and negatively correlated to the training volume, being lowered as the training volume was higher (Fig 2A -2D).Interestingly, the relative PRE-POST changes in CoP lenght induced by M1 stimulation was significantly correlated to the initial CoP length (PRE-data) for unipedal stance only (Fig 2F).

Discussion
The effect of two different montage of tDCS on postural control of Parkour athletes has been monitored by analyzing the CoP characteristics in static and dynamic tasks.An acute session of tDCS applied to M1 led to significant reduction of CoP movements for unipedal and bipedal stances while dlPFC or SHAM stimulation did not.This decrease was negatively correlated to the experience of the participants, i.e. lower for the most trained athletes.

Neurophysiological mechanisms
It has been shown that anodal stimulation of dlPFC could lead to an improvement of postural control, in younger healthy subject [14].The result of the present study did not meet the initial hypothesis since no effect has been found in parkour practitioners.A possible explanation of this lack of results could probably be linked to the convergence of two factors: 1) parkour athletes present already high balance abilities 2) the dlPFC is not the most involved area in posture.Indeed, traceurs demonstrated strong abilities to maintain posture at least in the tested tasks [17], making the room for improvement far less important than in recreationally active participants.Therefore, although the dlPFC do have a role in managing standing balance [15], its role remains minor as compared to other brain region.The dlPFC is known to play a role in motor planning [29], and its stimulation was shown to be effective in modulating accurate pointing performances in parkour practitioners [12].From the present result, regarding posture it seems that parkour athletes would need a stronger stimulus.
On the contrary and in line with previous results on healthy young recreationally active participants [4,6,30,31], anodal M1 stimulation had a positive effect on balance control.M1 stimulation would be associated with neurophysiological changes over several hours [32] corresponding to an increase in the motor region excitability which would prevent decline in downward neural control.tDCS would also be able to modulate the motor cortical transmitter system by decreasing the activity of the gamma-aminobutyric acid (GABA)-ergic system [33], whose primary function is to inhibit nerve impulses.tDCS applied to M1 would therefore strengthen postural control by its ability to request more neural networks of the sensorimotor system [7,34].In addition, this trial adopted an extracephalic montage, which maximizes the effect of tDCS over the anode and can imply the modulation of a larger neural path [12], including subcortical structures involved in postural control [34].Thus, the neural activation of muscles engaged in maintaining balance would be more efficient, which could justify the reduction of CoP displacements for static stance.As previously stated, traceurs showed a greater cortico-spinal excitability and a different spinal/cortical activation pattern as compared to untrained individuals [20].Indeed, traceurs exhibit greater corticospinal excitability of  lower limb muscles, but lower spinal excitability, as compared to untrained participants.tDCS intervention on M1, but not on dlPFC, was shown to modulate cortical descending command and spinal excitability of traceurs [23].The particularly low level of soleus spinal excitability of traceurs, even as compared to other sport populations such as gymnasts [22], may make them particularly prone to respond to M1 tDCS intervention.Indeed, since soleus muscle is one of the most important effectors of static balance, this would explain the neurophysiological mechanisms behind M1 tDCS efficiency, particularly in this population.However, M1 stimulation did not produce comparable results from bipedal to unipedal balance.Even if the decrease of both CoP length and area was significant for both bipedal and unipedal conditions, this was not the case for medio-lateral (ML) displacements, for which the PRE-POST difference was significantly higher in unipedal condition only.More precisely, unipedal stance showed an increase in the ML movements after stimulation, while those made in the postero-anterior (PA) axis were reduced.This result was not expected but could finally attest for a change in postural control strategy [35].Unipedal balance requiring offsetting movements, decreasing sway on the PA axis could lead to a strong increase of ML oscillations.Unipedal balance involves tightening the calf muscles-sural triceps including gastrocnemii and soleus muscles-to reduce PA displacements or contracting the foot soles and ankles stabilizing muscles, such as the peroneus longus, to limit movements along the ML axis.These two coping strategies do not appear during the bipedal balance.
Considered the reference posture in humans, standing position offers better stability given that the support polygon in which we are involved is larger.Moreover, our results clearly showed that the amplitude of displacements on both axes was less important during bipedal condition (Fig 1E and 1F).These findings agree with a previous research, where larger PA movements were detected when keeping posture became less easy [36].Bipedal posture may then not be sufficiently sensitive to small variations such as those induced by tDCS, particularly in well-trained athletes.Unipedal standing seemed to represent a more complex task, allowing to discriminate the effect of tDCS.Indeed, for instance the ellipse of CoP displacement was nearly 5 times wider in unipedal stance than in bipedal stance.Stimulating M1 had then a wide field of action to enhance the characteristics of CoP in unilateral task (Fig 2F).Motor abilities and particularly postural strategies can become more effective with training and practice [37].Therefore, even with a good initial performance in balance, tDCS was efficient to modulate unipedal stance in well trained athletes.This possibly means that tDCS similarly affected uni-and bi-pedal strategies.

tDCS and targeted population
tDCS's impact varied depending on the level of expertise of the participants.The systematic review of Brachman et al., 2017 concluded that balance training was an effective tool in improving postural control [38].Holding balance is therefore at the center of training which justifies that the most experienced traceurs showed a lower CoP length and area.Parkour practitioners already demonstrated a significant better postural control performance than sedentary people during landing [21].The effects of physical activity on postural control depends on the time of practice [39].Traceurs, therefore, represent a population on which brain stimulation is effective on postural balance through the stimulation of pre-existing neural networks.However, a ceiling effect can be reached for more experienced practitioners.When carefully looking at individual data, it can be observed that for some individuals the CoP length did not decrease after M1 tDCS.Therefore, a limit can be established between those who showed a significant downward modulation of CoP length after tDCS (n = 15/18 for bipedal stance and n = 12/18 for unipedal stance) for and those who did not (n = 3/18 for bipedal stance and n = 6/18 for unipedal stance).According to the training volume of these participants, the limit could be established between 6000 hours (for unipedal stance) and 8000 hours of training (for bipedal stance).In fact, the more the subject is trained, the less room there is for improvement.Finally, it can also be noticed that a great inter and intra-subject variability was reported regarding corticospinal excitability modulation following tDCS, which can be linked with a lack of knowledge concerning the current transfer location [40].Besides participants' expertise in the applied tasks, the effects of tDCS may also be affected by other intrinsic factors such as individual anatomic variations [41].
Practical implications and future directions.Parkour balance demand might be very specific, more than other sports requiring jumps such as basketball or volleyball.Indeed, traceurs' neuromuscular characteristics and especially the spinal excitability of calf muscles, main muscles responsible for static postural control, are more closed to ballet dancer [42].Indeed, the low spinal excitability of soleus muscle shown in traceurs was attributed both to the explosive demand (type II fast motor units) and to the particular motor control demand [20,22].Indeed, parkour requires not only to jump high or far, but to be accurate at the same time (e.g. when jumping from one the edge of a wall to another), making the activity fundamentally different from many other sports, such as track and field were the goal in to jump as far as possible [18].This conflict between power and accuracy may lead traceurs to show neurophysiological specificities, at a spinal level regarding reflex pathways as well as at cortical level in M1 area configuration [20].This may explain why acute tDCS applied over M1 might lead to jump enhancement in traceurs [23] but not in volleyball players for instance [43].Overall, literature suggests that acute tDCS intervention present some benefits if participants have expertise in the tested task [25].It seems that accurate motor control led participants to respond more to interventions such as non-invasive brain stimulation.However, in other populations an improvement in fine motor control or motor learning was not always observed after M1 tDCS intervention [44].The heterogeneity of the protocols, in terms of populations tested, outcomes, tDCS montage and settings, might be one of the main explanation for the large variability of the results observed in the literature about tDCS and balance.Furthermore, tDCS seems to be an intervention that needs to gather specific conditions to be effective, which are not yet determined.Particularly, future research focusing on the effect of tDCS on postural control of different trained and untrained population, associated to different balance outcomes (dynamic tests) might help to answer these research questions.Without inviting sport coaches to use such technological methods to improve motor performance, especially because the ethical and moral aspects of tDCS remain under debate [45,46], some practical recommendations can still be extracted from the present study.First, coaches should never neglect the neural component of sport performance.Indeed, an intervention at brain level can still have effects on physical performances.Here, tDCS was applied passively while participants were seated, and still improved some aspects of postural motor control.Second, there is an importance of the type and sensitivity of tested performance.Indeed, in the present study, unipedal test was more sensitive to tDCS application than bipedal test.It is important to choose a test that is discriminant enough to detect the efficacy of such neural enhancement method, which provide very targeted effects.Finally, the experience of participants might make them more or less responder to an intervention such as tDCS.As it is for usual physical preparation, sport professionals should always seek to individualize brain intervention according to the level of expertise.Future research comparing dose-effect responses of different brain stimulation techniques according to the level of expertise, might enhance our knowledge on how to implement such techniques in the field.

Conclusion
To summarize, the results of our study suggest that offline M1 stimulation with an extracephalic montage was suitable to improve postural control in Parkour practitioners, contrary to dlPFC stimulation.Among other intrinsic factors, we found that the effects of tDCS were correlated with participants' expertise in Parkour, as expressed by their total training volume.Then, although tDCS seems to be effective in modulating postural control in trained individuals, this technique may have limitations in the most highly trained of them.

Fig 2 .
Fig 2. Relationships between experience and CoP characteristics during static stance.A, C, E: Bidepal recordings.Initial CoP performances represent the averaged pre value by participants, before any tDCS intervention.B, D, F: Unipedal recordings.In E and F, the relative pre-post evolution of CoP with M1 tDCS are plotted against the initial CoP lenght value for bipedal and unipedal recordings, respectively.The relative changes in CoP variables with the M1 tDCS intervention is determined in percentage by the following formula: [(pre-post)/pre]*100).https://doi.org/10.1371/journal.pone.0286443.g002 seconds up to 2 mA (ramp-up), as recommended by previous literature (Gandiga et al., 2006; Moreira et al., 2021; Swann et al., 2015)